An Unusual Mortality Event of Florida Manatees is Related to Brevetoxin Exposure Through Ingestion of Seagrass
Florida Fish and Wildlife Conservation Commission, Florida Marine Research Institute
St. Petersburg, FL, USA
Abstract
From March 15 to April 30, 2002 there was a marked increase in the number of Florida manatee (Trichechus manatus latirostris) carcasses recovered in Southwest Florida, extending from Pinellas County south through Collier County. A Karenia brevis red tide had earlier been present in the area, but cell counts above baseline had not been detected since late January. Despite a lack of K. brevis cells in the water near where carcasses were found, gross findings in almost all manatees examined were consistent with, but not specific for, brevetoxicosis. The five fresh animals necropsied between March 15 and 26, exhibited marked congestion in the kidneys, liver, meninges, nasal mucosa, lungs, airways, and mandibular and axillary lymph nodes. A few animals had pulmonary edema. With the exception of presumptive enteritis, and possible subdural hemorrhage, there was no evidence of an infectious or inflammatory disease or of trauma in these animals.
A suite of tissues including liver, kidney, lung, urine, stomach contents, and occasionally heart, fat, and brain, was collected from most animals at necropsy. Tissue samples were analyzed for brevetoxins using an ELISA assay. Tissues from animals collected in non-red tide regions of Florida served as negative controls. Of 42 carcasses recovered, 30 tested positive for brevetoxins in more than one tissue. Three additional, severely decomposed animals for which tissues were not available were considered part of the event due to their carcass recovery location. Brevetoxin concentrations were highest in stomach contents (max. 1,132ng/g) then liver (max. 300 ng/g), kidney, lung and urine. Brevetoxins were not detected in tissues from animals outside of southwest Florida. In addition, the five carcasses recovered in southwest Florida during May 2002 had background brevetoxin concentrations below detectable concentrations (<5ng/g).
Brevetoxins produced by K. brevis have previously been associated with mass mortalities of manatees in Florida. In 1996 the primary exposure route appeared to be through the inhalation of aerosolized brevetoxins, and in 1982, through the ingestion of toxic filter feeding organisms, such as tunicates. Detectable red tide blooms at high concentrations were present in the area concurrently with the mortality event in 1996,1 and just preceding the 1982 event.2 Because above background K. brevis cells had not been detected in the water for over a month in the area where the manatees died, we questioned the exposure mechanism of manatees to brevetoxin during this unusual mortality. Seagrass, sediment and water samples were collected and brevetoxins analyzed biweekly from March 28 through June 20 near four sites where carcasses had been recovered and at one control site where there had been no mortality. The four sites where carcasses were recovered consistently tested positive for brevetoxins in all three sample types, with seagrass having the highest concentrations (max. 1,263ng/g whole seagrass on June 20) followed by sediment (max. 62ng/g on March 28) and seawater (max. 1.28ng/g on April 25). Seagrass components were separated and analyzed individually. Scrapings of epiphytes contained high levels of brevetoxins (max. 2,907ng/g on June 20) followed by rhizomes (max. 189ng/g on April 11), blades (max. 77ng/g on May 9), and sheaths (max. 70ng/g on April 11). Brevetoxins were not detected at the control site.
These results confirm the stability of brevetoxins in the environment in the absence of an ongoing K. brevis bloom. They also demonstrate the chronic risk of manatees to brevetoxins through an indirect exposure route. This is the first time that a significant number of manatee deaths have been related to the ingestion of brevetoxin via seagrass and associated epiphytes during a non-red tide event. The confirmation of brevetoxins in these animals continues to demonstrate the far-reaching impacts of Florida red tides on the manatee population.
Acknowledgements
This work was supported by the Save the Manatee Trust Fund and by a grant from the U.S. Fish and Wildlife Service. Research is conducted under USFWS permit MA773494-6 issued to the Florida Marine Research Institute. Jim Valade (USFWS) provided valuable assistance as the federal on-site coordinator for this unusual marine mammal mortality event. Thanks to the entire team at FMRI who responded to this event.
References
1. Bossart GD, DG Baden, RY Ewing, B Roberts, SD Wright. 1998. Brevetoxicosis in manatees (Trichechus manatus latirostris) from the 1996 epizootic: gross, histologic and immunohistochemical features. Toxicologic Pathology 26: 276-282.
2. O'Shea TJ, GB Rathbun, RK Bonde, CD Buergelt, DK Odell. 1991. An epizootic of Florida manatees associated with a dinoflagellate bloom. Marine Mammal Science 7: 165-179.